Understanding mutualism when there is adaptation to the partner

1 A mutualism is a mutually beneficial interaction between individuals of two species. Here we show that the degree of benefit resulting from an interaction depends on whether adaptation within the mutualism is considered. 2 A species'proximate response measures the short-term effect of addition or removal of the partner species, without allowing for any adaptation. We define a proximate mutualism as an interaction in which removal of each partner results in a decreased performance of the other, i.e. both species show a positive proximate response to the presence of the partner. 3 A proximate mutualism might, however, only reflect evolved dependence (i.e. the species has lost its ability to perform well without the partner). Some authors therefore insist on an ultimate criterion, regardless of the use of proximate responses in almost all empirical studies. 4 A species'ultimate response measures the long-term effect of adding or removing the partner species, thus allowing the focal species to adapt. In an ultimate mutualism neither partner could ever have performed as well without the other. In other words, a mutualism is called ultimate if both species show a positive ultimate response to the presence of the partner. Despite the conceptual attractiveness of this definition, ultimate responses are difficult to measure, rendering its use operationally problematic. 5 Mutualistic evolution, the evolution of a trait that is costly to the bearer but beneficial to its partner, is not, paradoxically, a necessary consequence of either proximate or ultimate mutualism. Another counterintuitive result is that even obligate mutualisms are not necessarily ultimate interactions. 6 We conclude that the proximate response is the only workable criterion for mutualism. Our understanding of mutualism, however, requires further evaluation of how evolved dependence may be responsible for such responses. 7 These concepts clarify the ongoing debate about whether plant-herbivore interactions can be considered as mutualistic. 8 This is not a semantic case of hair splitting: naive aspects in current views of mutualism need revision. In most, if not all, interactions now considered as mutualisms, some of the measured benefits are likely to result from evolved dependence, rather than what we would like to consider as ultimate benefits.